Distinct terminal and cell body mechanisms in the nociceptor mediate hyperalgesic priming

Journal of Neuroscience

Volumn 35, Issue 15, 2015, Pages 6107-6116

  Ferrari, Luiz F ^a   Araldi, Dioneia ^a   Levine, Jon D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dorsal root ganglion; Hyperalgesic priming; Mechanical hyperalgesia; Nociceptor; Rat

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; KARYOPHERIN; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NERVE GROWTH FACTOR; PROSTAGLANDIN E2; PROTEIN KINASE C; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR ALPHA; 8 BROMO CYCLIC AMP; ANTISENSE OLIGODEOXYNUCLEOTIDE; CCL2 PROTEIN, RAT; DACTINOMYCIN; PROTEIN KINASE C EPSILON;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; DOWN REGULATION; GENETIC TRANSCRIPTION; HEAT PAIN THRESHOLD; HYPERALGESIA; IMMUNOFLUORESCENCE TEST; MALE; NERVE ENDING; NONHUMAN; PAIN RECEPTOR; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL GANGLION; ADVERSE EFFECTS; ANIMAL; CYTOLOGY; DISEASE MODEL; DRUG ADMINISTRATION ROUTE; DRUG EFFECTS; GENETICS; METABOLISM; PAIN THRESHOLD; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; STIMULATION;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CHEMOKINE CCL2; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DACTINOMYCIN; DINOPROSTONE; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION ROUTES; GANGLIA, SPINAL; HYPERALGESIA; MALE; NOCICEPTORS; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; PAIN THRESHOLD; PHYSICAL STIMULATION; PROTEIN KINASE C-EPSILON; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84929248550     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5085-14.2015     Document Type: Article

References (69)

1. Ahluwalia A, Jones MK, Szabo S, Tarnawski AS (2014) Aging impairs transcriptional regulation of vascular endothelial growth factor in human microvascular endothelial cells: implications for angiogenesis and cell survival. J Physiol Pharmacol 65:209-215. Medline
2. Aley KO, Levine JD (1999) Role of protein kinase A in the maintenance of inflammatory pain. J Neurosci 19:2181-2186. Medline
3. Aley KO, Messing RO, Mochly-Rosen D, Levine JD (2000) Chronic hypersensitivity for inflammatory nociceptor sensitization mediated by the epsilon isozyme of protein kinase C. J Neurosci 20:4680-4685. Medline
4. Alvarez P, Green PG, Levine JD (2014) Role for monocyte chemoattractant protein-1 in the induction of chronic muscle pain in the rat. Pain 155: 1161-1167. CrossRef Medline
5. American College of Rheumatology (2000) Recommendations for the medical management of osteoarthritis of the hip and knee: 2000 update. American College of Rheumatology Subcommittee on Osteoarthritis Guidelines. Arthritis Rheum 43:1905-1915. CrossRef Medline
6. Araldi D, Ferrari LF, Lotufo CM, Vieira AS, Athié MC, Figueiredo JG, Duarte DB, Tambeli CH, Ferreira SH, Parada CA (2013) Peripheral inflammatory hyperalgesia depends on the COX increase in the dorsal root ganglion. Proc Natl Acad Sci U S A 110:3603-3608. CrossRef Medline
7. Bingham CO 3rd (2002) Development and clinical application of COX-2-selective inhibitors for the treatment of osteoarthritis and rheumatoid arthritis. Cleve Clin J Med 69 [Suppl 1]:SI5-SI12. Medline
8. Bogen O, Alessandri-Haber N, Chu C, Gear RW, Levine JD (2012) Generation of a pain memory in the primary afferent nociceptor triggered by PKCε activation of CPEB. J Neurosci 32:2018-2026. CrossRef Medline
9. Borle AB, Snowdowne KW (1982) Measurement of intracellular free calcium in monkey kidney cells with aequorin. Science 217:252-254. CrossRef Medline
10. Burch RM, Axelrod J (1987) Dissociation of bradykinin-induced prosta glandin formation from phosphatidylinositol turnover in Swiss 3T3 fibroblasts: evidence for G protein regulation of phospholipase A2. Proc Natl Acad Sci USA 84:6374-6378. CrossRef Medline
11. Chen L, Yang G, Grosser T (2013) Prostanoids and inflammatory pain. Prostaglandins Other Lipid Mediat 104-105:58-66. CrossRef Medline
12. Chidlow G, Ebneter A, Wood JP, Casson RJ (2011) The optic nerve head is the site of axonal transport disruption, axonal cytoskeleton damage and putative axonal regeneration failure in a rat model of glaucoma. Acta Neuropathol 121:737-751. CrossRef Medline
13. Churn SB, Sombati S, Jakoi ER, Severt L, DeLorenzo RJ, Sievert L (2000) Inhibition of calcium/calmodulin kinase II alpha subunit expression results in epileptiform activity in cultured hippocampal neurons. Proc Natl Acad Sci USA 97:5604-5609. CrossRef Medline
14. Dina OA, Green PG, Levine JD (2008) Role of interleukin-6 in chronic muscle hyperalgesic priming. Neuroscience 152:521-525. CrossRef Medline
15. Dina OA, Khasar SG, Gear RW, Levine JD (2009) Activation of Gi induces mechanical hyperalgesia poststress or inflammation. Neuroscience 160:501-507. CrossRef Medline
16. El Bahri DM, Meddeb N, Sellami S (2007) Rheumatoid arthritis: current status of therapy. Tunis Med 85:1-8. Medline
17. Feldmann M, Maini RN (2001) Anti-TNF alpha therapy of rheumatoid arthritis: what have we learned? Annu Rev Immunol 19:163-196. CrossRef Medline
18. Ferrari LF, Cunha FQ, Parada CA, Ferreira SH (2007) A novel technique to perform direct intraganglionar injections in rats. J Neurosci Methods 159:236-243. CrossRef Medline
19. Ferrari LF, Bogen O, Levine JD (2010) Nociceptor subpopulations involved in hyperalgesic priming. Neuroscience 165:896-901. CrossRef Medline
20. Ferrari LF, Bogen O, Alessandri-Haber N, Levine E, Gear RW, Levine JD (2012) Transient decrease in nociceptor GRK2 expression produces long-term enhancement in inflammatory pain. Neuroscience 222:392-403. CrossRef Medline
21. Ferrari LF, Levine E, Levine JD (2013a) Role of a novel nociceptor autocrine mechanism in chronic pain. Eur J Neurosci 37:1705-1713. CrossRef Medline
22. Ferrari LF, Bogen O, Levine JD (2013b) Role of nociceptor αCaMKII in transition from acute to chronic pain (hyperalgesic priming) in male and female rats. J Neurosci 33:11002-11011. CrossRef Medline
23. Ferrari LF, Bogen O, Chu C, Levine JD (2013c) Peripheral administration of translation inhibitors reverses increased hyperalgesia in a model of chronic pain in the rat. J Pain 14:731-738. CrossRef Medline
24. Ferrari LF, Bogen O, Levine JD (2014) Second messengers mediating the expression of neuroplasticity in a model of chronic pain in the rat. J Pain 15:312-320. CrossRef Medline
25. Ferrari LF, Bogen O, Reichling DB, Levine JD (2015) Accounting for the delay in the transition from acute to chronic pain: axonal and nuclear mechanisms. J Neurosci 35:495-507. CrossRef Medline
26. Ferreira SH (1972) Prostaglandins, aspirin-like drugs and analgesia. Nat New Biol 240:200-203. CrossRef Medline
27. Forwood JK, Lam MH, Jans DA (2001) Nuclear import of Creb and AP-1 transcription factors requires importin-beta 1 and Ran but is independent of importin-alpha. Biochemistry 40:5208-5217. CrossRef Medline
28. Fraser JE, Rawlinson SM, Wang C, Jans DA, Wagstaff KM (2014) Investigating dengue virus nonstructural protein 5 (NS5) nuclear import. Methods Mol Biol 1138:301-328. CrossRef Medline
29. Gniazdowski M, Denny WA, Nelson SM, Czyz M (2003) Transcription factors as targets for DNA-interacting drugs. Curr Med Chem 10:909-924. CrossRef Medline
30. Hayashi Y, Kuroda T, Kishimoto H, Wang C, Iwama A, Kimura K (2014) Downregulation of rRNA transcription triggers cell differentiation. PLoS One 9:e98586. CrossRef Medline
31. Hochberg MC, Altman RD, April KT, Benkhalti M, Guyatt G, McGowan J, Towheed T, Welch V, Wells G, Tugwell P (2012) American College of Rheumatology 2012 recommendations for the use of nonpharmacologic and pharmacologic therapies in osteoarthritis of the hand, hip, and knee. Arthritis Care Res (Hoboken) 64:465-474. Medline
32. Johnson JA, Gray MO, Chen CH, Mochly-Rosen D (1996) A protein kinase C translocation inhibitor as an isozyme-selective antagonist of cardiac function. J Biol Chem 271:24962-24966. CrossRef Medline
33. Joseph EK, Levine JD (2010) Hyperalgesic priming is restricted to isolectin B4-positive nociceptors. Neuroscience 169:431-435. CrossRef Medline
34. Joseph EK, Bogen O, Alessandri-Haber N, Levine JD (2007) PLC-beta 3 signals upstream of PKC epsilon in acute and chronic inflammatory hyperalgesia. Pain 132:67-73. CrossRef Medline
35. Kapoor M, Shaw O, Appleton I (2005) Possible anti-inflammatory role of COX-2-derived prostaglandins: implications for inflammation research. Curr Opin Investig Drugs 6:461-466. Medline
36. Khasar SG, Lin YH, Martin A, Dadgar J, McMahon T, Wang D, Hundle B, Aley KO, Isenberg W, McCarter G, Green PG, Hodge CW, Levine JD, Messing RO (1999) A novel nociceptor signaling pathway revealed in protein kinase C epsilon mutant mice. Neuron 24:253-260. CrossRef Medline
37. Khasar SG, Green PG, Levine JD (2005) Repeated sound stress enhances inflammatory pain in the rat. Pain 116:79-86. CrossRef Medline
38. Khasar SG, Burkham J, Dina OA, Brown AS, Bogen O, Alessandri-Haber N, Green PG, Reichling DB, Levine JD (2008) Stress induces a switch of intracellular signaling in sensory neurons in a model of generalized pain. J Neurosci 28:5721-5730. CrossRef Medline
39. Khasar SG, Dina OA, Green PG, Levine JD (2009) Sound stress-induced long-term enhancement of mechanical hyperalgesia in rats is maintained by sympathoadrenal catecholamines. J Pain 10:1073-1077. CrossRef Medline
40. Kozyrev SA, Nikitin VP (2013) Involvement of translation and transcription processes into neurophysiological mechanisms of long-term memory reconsolidation. Bull Exp Biol Med 154:584-587. CrossRef Medline
41. Lane-Ladd SB, Pineda J, Boundy VA, Pfeuffer T, Krupinski J, Aghajanian GK, Nestler EJ (1997) CREB (cAMP response element-binding protein) in the locus ceruleus: biochemical, physiological, and behavioral evidence for a role in opiate dependence. J Neurosci 17:7890-7901. Medline
42. Lokich E, Singh RK, Han A, Romano N, Yano N, Kim K, Moore RG (2014) HE4 expression is associated with hormonal elements and mediated by importin-dependent nuclear translocation. Sci Rep 4:5500. CrossRef Medline
43. Lund LM, Machado VM, McQuarrie IG (2005) Axonal isoforms of myosin-I. Biochem Biophys Res Commun 330:857-864. CrossRef Medline
44. Ma W, Hatzis C, Eisenach JC (2003) Intrathecal injection of cAMP response element binding protein (CREB) antisense oligonucleotide attenuates tactile allodynia caused by partial sciatic nerve ligation. Brain Res 988:97-104. CrossRef Medline
45. Martel-Pelletier J, Pelletier JP, Fahmi H (2003) Cyclooxygenase-2 and prostaglandins in articular tissues. Semin Arthritis Rheum 33:155-167. CrossRef Medline
46. Miao FJ, Green PG, Benowitz N, Levine JD (2004) Central terminals of nociceptors are targets for nicotine suppression of inflammation. Neuroscience 123:777-784. CrossRef Medline
47. Ochi T, Ohkubo Y, Mutoh S (2003) Role of cyclooxygenase-2, but not cyclooxygenase-1, on type II collagen-induced arthritis in DBA/1J mice. Biochem Pharmacol 66:1055-1060. CrossRef Medline
48. Ouseph AK, Khasar SG, Levine JD (1995) Multiple second messenger systems act sequentially to mediate rolipram-induced prolongation of prostaglandin E2-induced mechanical hyperalgesia in the rat. Neuroscience 64:769-776. CrossRef Medline
49. Parada CA, Yeh JJ, Joseph EK, Levine JD (2003a) Tumor necrosis factor receptor type-1 in sensory neurons contributes to induction of chronic enhancement of inflammatory hyperalgesia in rat. Eur J Neurosci 17: 1847-1852. CrossRef Medline
50. Parada CA, Yeh JJ, Reichling DB, Levine JD (2003b) Transient attenuation of protein kinase Cepsilon can terminate a chronic hyperalgesic state in the rat. Neuroscience 120:219-226. CrossRef Medline
51. Parada CA, Reichling DB, Levine JD (2005) Chronic hyperalgesic priming in the rat involves a novel interaction between cAMP and PKCepsilon second messenger pathways. Pain 113:185-190. CrossRef Medline
52. Quanhong Z, Ying X, Moxi C, Tao X, Jing W, Xin Z, Li W, Derong C, Xiaoli Z, Wei J (2012) Intrathecal PLC(beta3) oligodeoxynucleotides antisense potentiates acute morphine efficacy and attenuates chronic morphine tolerance. Brain Res 1472:38-44. CrossRef Medline
53. Randall LO, Selitto JJ (1957) A method for measurement of analgesic activity on inflamed tissue. Arch Int Pharmacodyn Ther 111:409-419. Medline
54. Reichling DB, Levine JD (2009) Critical role of nociceptor plasticity in chronic pain. Trends Neurosci 32:611-618. CrossRef Medline
55. Ricciotti E, FitzGerald GA (2011) Prostaglandins and inflammation. Arterioscler Thromb Vase Biol 31:986-1000. CrossRef Medline
56. Shubayev VI, Myers RR (2001) Axonal transport of TNF-alpha in painful neuropathy: distribution of ligand tracer and TNF receptors. J Neuroimmunol 114:48-56. CrossRef Medline
57. Slońska A, Cymerys J, Skwarska J, Golke A, Bańbura MW (2013) Influence of importin alpha/beta and exportin 1 on equine herpesvirus type 1 (EHV-1) replication in primary murine neurons. Pol J Vet Sci 16:749-751. Medline
58. Song MJ, Wang YQ, Wu GC (2009) Additive anti-hyperalgesia of electroacupuncture and intrathecal antisense oligodeoxynucleotide to interleukin-1 receptor type I on carrageenan-induced inflammatory pain in rats. Brain Res Bull 78:335-341. CrossRef Medline
59. Su L, Wang C, Yu YH, Ren YY, Xie KL, Wang GL (2011) Role of TRPM8 in dorsal root ganglion in nerve injury-induced chronic pain. BMC Neurosci 12:120. CrossRef Medline
60. Sun JL, Xiao C, Lu B, Zhang J, Yuan XZ, Chen W, Yu LN, Zhang FJ, Chen G, Yan M (2013) CX3CL1/CX3CR1 regulates nerve injury-induced pain hypersensitivity through the ERK5 signaling pathway. J Neurosci Res 91: 545-553. CrossRef Medline
61. Taiwo YO, Levine JD (1989) Prostaglandin effects after elimination of indirect hyperalgesic mechanisms in the skin of the rat. Brain Res 492:397-399. CrossRef Medline
62. Taiwo YO, Coderre TJ, Levine JD (1989) The contribution of training to sensitivity in the nociceptive paw-withdrawal test. Brain Res 487:148-151. CrossRef Medline
63. Taiwo YO, Heller PH, Levine JD (1990) Characterization of distinct phospholipases mediating bradykinin and noradrenaline hyperalgesia. Neuroscience 39:523-531. CrossRef Medline
64. Tambeli CH, Parada CA, Levine JD, Gear RW (2002) Inhibition of tonic spinal glutamatergic activity induces antinociception in the rat. Eur J Neurosci 16:1547-1553. CrossRef Medline
65. Wagstaff KM, Sivakumaran H, Heaton SM, Harrich D, Jans DA (2012) Ivermectin is a specific inhibitor of importin alpha/beta-mediated nuclear import able to inhibit replication of HIV 1 and dengue virus. Biochem J 443:851-856. CrossRef Medline
66. Widnell KL, Self DW, Lane SB, Russell DS, Vaidya VA, Miserendino MJ, Rubin CS, Duman RS, Nestler EJ (1996) Regulation of CREB expression: in vivo evidence for a functional role in morphine action in the nucleus accumbens. J Pharmacol Exp Ther 276:306-315. Medline
67. Wiegert JS, Hofmann F, Bading H, Bengtson CP (2009) A transcription-dependent increase in miniature EPSC frequency accompanies late-phase plasticity in cultured hippocampal neurons. BMC Neurosci 10:124. CrossRef Medline
68. Woolf CJ (2010) What is this thing called pain? J Clin Invest 120:3742-3744. CrossRef Medline
69. Wu W, Toma JG, Chan H, Smith R, Miller FD (1994) Disruption of fast axonal transport in vivo leads to alterations in Schwann cell gene expression. Dev Biol 163:423-439. CrossRef Medline